Hydra and the evolution of stem cells

Hydra are remarkable because they are immortal. Much of immortality can be ascribed to the asexual mode of reproduction by budding, which requires a tissue consisting of stem cells with continuous self‐renewal capacity. Emerging novel technologies and the availability of genomic resources enable for the first time to analyse these cells in vivo. Stem cell differentiation in Hydra is governed through the coordinated actions of conserved signaling pathways. Studies of stem cells in Hydra, therefore, promise critical insights of general relevance into stem cell biology including cellular senescence, lineage programming and reprogramming, the role of extrinsic signals in fate determination and tissue homeostasis, and the evolutionary origin of these cells. With these new facts as a backdrop, this review traces the history of studying stem cells in Hydra and offers a view of what the future may hold.

[1]  T. Bosch,et al.  Plasticity of epithelial cell shape in response to upstream signals: a whole-organism study using transgenic Hydra. , 2009, Zoology.

[2]  B. Edgar,et al.  Proliferative control in Drosophila stem cells. , 2008, Current opinion in cell biology.

[3]  T. Bosch,et al.  Compagen, a comparative genomics platform for early branching metazoan animals, reveals early origins of genes regulating stem‐cell differentiation , 2008, BioEssays : news and reviews in molecular, cellular and developmental biology.

[4]  A. Sánchez Alvarado,et al.  Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. , 2008, Cell stem cell.

[5]  K. Agata,et al.  Brain regeneration from pluripotent stem cells in planarian , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[6]  G. Sauvageau,et al.  Polycomb Group Genes: Keeping Stem Cell Activity in Balance , 2008, PLoS biology.

[7]  T. Misteli,et al.  Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing , 2008, Nature Cell Biology.

[8]  H. le Guyader,et al.  Ordered progression of nematogenesis from stem cells through differentiation stages in the tentacle bulb of Clytia hemisphaerica (Hydrozoa, Cnidaria). , 2008, Developmental biology.

[9]  I. Weissman,et al.  Stems Cells and the Pathways to Aging and Cancer , 2008, Cell.

[10]  Leonard Hayflick,et al.  Entropy Explains Aging, Genetic Determinism Explains Longevity, and Undefined Terminology Explains Misunderstanding Both , 2007, PLoS genetics.

[11]  C. Patrick Doncaster,et al.  Density Dependence Triggers Runaway Selection of Reduced Senescence , 2007, PLoS Comput. Biol..

[12]  M. Wallenfang,et al.  Aging within the Stem Cell niche. , 2007, Developmental cell.

[13]  D. Arendt,et al.  Vasa unveils a common origin of germ cells and of somatic stem cells from the posterior growth zone in the polychaete Platynereis dumerilii. , 2007, Developmental biology.

[14]  A. Böttger,et al.  The Notch signaling pathway in the cnidarian Hydra. , 2007, Developmental biology.

[15]  T. Gojobori,et al.  Degeneration after sexual differentiation in hydra and its relevance to the evolution of aging. , 2006, Gene.

[16]  H. Watanabe,et al.  The Wnt code: cnidarians signal the way , 2006, Oncogene.

[17]  D. Scadden,et al.  The stem-cell niche as an entity of action , 2006, Nature.

[18]  J. Lohmann,et al.  Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[19]  T. Bosch,et al.  Discovery of genes expressed in Hydra embryogenesis. , 2006, Developmental biology.

[20]  H. Bode,et al.  Formation of the head organizer in hydra involves the canonical Wnt pathway , 2005, Development.

[21]  U. Frank,et al.  Totipotent migratory stem cells in a hydroid. , 2004, Developmental biology.

[22]  A. Mclaren,et al.  Primordial germ cells in the mouse. , 2003, Developmental biology.

[23]  T. Fujisawa,et al.  Polyps, peptides and patterning , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

[24]  A. Spradling,et al.  A niche maintaining germ line stem cells in the Drosophila ovary. , 2000, Science.

[25]  Christoph M. Happel,et al.  WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra , 2000, Nature.

[26]  H. Bode,et al.  A novel neuropeptide, Hym-355, positively regulates neuron differentiation in Hydra. , 1999, Development.

[27]  D. Martinez,et al.  Mortality Patterns Suggest Lack of Senescence in Hydra , 1998, Experimental Gerontology.

[28]  A. Spradling,et al.  A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. , 1997, Development.

[29]  C. Nishimiya-Fujisawa,et al.  Genetic analysis of developmental mechanisms in Hydra. XXII. Two types of female germ stem cells are present in a male strain of Hydra magnipapillata. , 1995, Developmental biology.

[30]  C. Nishimiya-Fujisawa,et al.  Genetic analysis of developmental mechanisms in hydra. XX. Cloning of interstitial stem cells restricted to the sperm differentiation pathway in Hydra magnipapillata. , 1993, Developmental biology.

[31]  H. Lenhoff Ethel Browne, Hans Spemann, and the Discovery of the Organizer Phenomenon. , 1991, The Biological bulletin.

[32]  T. Fujisawa,et al.  Transplantation stimulates interstitial cell migration in hydra. , 1990, Developmental biology.

[33]  T. Bosch,et al.  Cloned interstitial stem cells grow as contiguous patches in hydra. , 1990, Developmental biology.

[34]  T. Bosch,et al.  Stem cells of Hydra magnipapillata can differentiate into somatic cells and germ line cells , 1987 .

[35]  T. Bosch,et al.  Male and female stem cells and sex reversal in Hydra polyps. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[36]  H. Bode,et al.  Growth regulation of the interstitial cell population in hydra. III. Interstitial cell density does not control stem cell proliferation. , 1986, Developmental biology.

[37]  H. Bode,et al.  Growth regulation of the interstitial cell population in hydra. I. Evidence for global control by nerve cells in the head. , 1986, Developmental biology.

[38]  C. Littlefield Germ cells in Hydra oligactis males. I. Isolation of a subpopulation of interstitial cells that is developmentally restricted to sperm production. , 1985, Developmental biology.

[39]  P. Tardent,et al.  Dynamics of hydra populations in Lake Zürich, Switzerland, and Lake Maggiore, Italy , 1985, Swiss journal of hydrology.

[40]  L. Buss,et al.  Histoincompatibility in vertebrates: the relict hypothesis. , 1985, Developmental and comparative immunology.

[41]  H. Bode,et al.  Interstitial cell migration in Hydra attenuata. I. Quantitative description of cell movements. , 1984, Developmental biology.

[42]  H. Bode,et al.  Formation of pattern in regenerating tissue pieces of Hydra attenuata. II. Degree of proportion regulation is less in the hypostome and tentacle zone than in the tentacles and basal disc. , 1984, Developmental biology.

[43]  C. N. David,et al.  Regulation of the self-renewal probability in Hydra stem cell clones. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[44]  H. Bode,et al.  Regulation of interstitial cell differentiation inHydra attenuata , 1977, Wilhelm Roux's archives of developmental biology.

[45]  C. N. David,et al.  Characterization of interstitial stem cells in hydra by cloning. , 1977, Developmental biology.

[46]  H. Bode,et al.  Constraints on the relative sizes of the cell populations in Hydra attenuata. , 1977, Journal of cell science.

[47]  P. Feldman Evolution of sex , 1975, Nature.

[48]  A. Gierer,et al.  Cell cycle kinetics and development of Hydra attenuata. III. Nerve and nematocyte differentiation. , 1974, Journal of cell science.

[49]  R. D. Campbell,et al.  Cell cycle kinetics and development of Hydra attenuata. II. Interstitial cells. , 1974, Journal of cell science.

[50]  P. Tardent Gametogenesis in the Genus Hydra , 1974 .

[51]  C. N. David,et al.  Distribution of Interstitial Cells and Differentiating Nematocytes in Nests in Hydra attenuata , 1974 .

[52]  A. Gierer,et al.  Regeneration of hydra from reaggregated cells. , 1972, Nature: New biology.

[53]  R. D. Campbell,et al.  Cell cycle kinetics and development of Hydra attenuata. I. Epithelial cells. , 1972, Journal of cell science.

[54]  R. D. Campbell,et al.  Tissue dynamics of steady state growth in Hydra littoralis. I. Patterns of cell division. , 1967, Developmental biology.

[55]  L. Hayflick THE LIMITED IN VITRO LIFETIME OF HUMAN DIPLOID CELL STRAINS. , 1965, Experimental cell research.

[56]  L. Hayflick,et al.  The serial cultivation of human diploid cell strains. , 1961, Experimental cell research.

[57]  H. Spemann,et al.  über Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren , 1924, Archiv für mikroskopische Anatomie und Entwicklungsmechanik.

[58]  Ethel Nicholson Browne,et al.  The production of new hydranths in Hydra by the insertion of small grafts , 1909 .

[59]  T. Bosch,et al.  Cell type complexity in the basal metazoan Hydra is maintained by both stem cell based mechanisms and transdifferentiation. , 2008, Developmental biology.

[60]  T. Bosch Symmetry breaking in stem cells of the basal metazoan Hydra. , 2007, Progress in molecular and subcellular biology.

[61]  U. Frank,et al.  An evolutionary conserved role of Wnt signaling in stem cell fate decision. , 2006, Developmental biology.

[62]  C. David,et al.  Role of the cellular environment in interstitial stem cell proliferation in Hydra , 2004, Roux's archives of developmental biology.

[63]  R. Lehmann,et al.  Germ cell development in Drosophila. , 1996, Annual review of cell and developmental biology.

[64]  L. Buss,et al.  The evolution of individuality , 1987 .

[65]  H. Bode,et al.  Regulation of interstitial cell differentiation in Hydra attenuata. I. Homeostatic control of interstitial cell population size. , 1976, Journal of cell science.

[66]  Abraham Trembley Mémoires, pour servir à l'histoire d'un genre de polypes d'eau douce, à bras en forme de cornes , 1975 .

[67]  August. Weismann,et al.  Das Keimplasma : eine Theorie der Vererbung , 1892 .

[68]  August. Weismann,et al.  Die Entstehung der Sexualzellen bei den Hydromedusen : zugleich ein Beitrag zur Kenntniss des Baues und der Lebenserscheinungen dieser Gruppe , 1883 .